Ly6Chi Monocytes in the Inflamed Colon Give Rise to Proinflammatory Effector Cells and Migratory Antigen-Presenting Cells

Immunity

Volumn 37, Issue 6, 2012, Pages 1076-1090

  Zigmond, Ehud ^a,b   Varol, Chen ^b   Farache, Julia ^a   Elmaliah, Elinor ^b   Satpathy, Ansuman T ^c   Friedlander, Gilgi ^a   Mack, Matthias ^d   Shpigel, Nahum ^e   Boneca, Ivo G ^f,g   Murphy, Kenneth M ^c   Shakhar, Guy ^a   Halpern, Zamir ^b   Jung, Steffen ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF REGENSBURG   (Germany)

^e HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^f INSTITUT PASTEUR   (France)

^g INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; CHEMOKINE RECEPTOR CCR2; TOLL LIKE RECEPTOR 2;

ANTIGEN PRESENTING CELL; ARTICLE; CELL FATE; CELL MIGRATION; COLITIS; CONTROLLED STUDY; EFFECTOR CELL; HUMAN; HUMAN CELL; LAMINA PROPRIA; MICROENVIRONMENT; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, LY; CELL MOVEMENT; COLITIS; DISEASE MODELS, ANIMAL; GENE EXPRESSION PROFILING; IMMUNOPHENOTYPING; MACROPHAGES; MICE; MICE, TRANSGENIC; MONOCYTES; NOD2 SIGNALING ADAPTOR PROTEIN; RECEPTORS, CCR2; RECEPTORS, CHEMOKINE; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 2;

EID: 84870900504     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.08.026     Document Type: Article

References (59)

1. Ajami B., Bennett J.L., Krieger C., McNagny K.M., Rossi F.M. Infiltrating monocytes trigger EAE progression, but do not contribute to the resident microglia pool. Nat. Neurosci. 2011, 14:1142-1149.
2. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 2008, 8:411-420.
3. Atarashi K., Tanoue T., Shima T., Imaoka A., Kuwahara T., Momose Y., Cheng G., Yamasaki S., Saito T., Ohba Y., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341.
4. Auffray C., Fogg D., Garfa M., Elain G., Join-Lambert O., Kayal S., Sarnacki S., Cumano A., Lauvau G., Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
5. Barnden M.J., Allison J., Heath W.R., Carbone F.R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 1998, 76:34-40.
6. Becker C., Fantini M.C., Neurath M.F. High resolution colonoscopy in live mice. Nat. Protoc. 2006, 1:2900-2904.
7. Bevins C.L., Salzman N.H. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat. Rev. Microbiol. 2011, 9:356-368.
8. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., Liu K., Jakubzick C., Ingersoll M.A., Leboeuf M., et al. Origin of the lamina propria dendritic cell network. Immunity 2009, 31:513-525.
9. Brühl H., Cihak J., Plachý J., Kunz-Schughart L., Niedermeier M., Denzel A., Rodriguez Gomez M., Talke Y., Luckow B., Stangassinger M., Mack M. Targeting of Gr-1+,CCR2+ monocytes in collagen-induced arthritis. Arthritis Rheum. 2007, 56:2975-2985.
10. Cerovic V., Houston S.A., Scott C.L., Aumeunier A., Yrlid U., Mowat A.M., Milling S.W. Intestinal CD103(-) dendritic cells migrate in lymph and prime effector T cells. Mucosal. Immunol. 2012.
11. Cheong C., Matos I., Choi J.H., Dandamudi D.B., Shrestha E., Longhi M.P., Jeffrey K.L., Anthony R.M., Kluger C., Nchinda G., et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell 2010, 143:416-429.
12. Cho J.H. The genetics and immunopathogenesis of inflammatory bowel disease. Nat. Rev. Immunol. 2008, 8:458-466.
13. Coombes J.L., Siddiqui K.R., Arancibia-Cárcamo C.V., Hall J., Sun C.M., Belkaid Y., Powrie F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 2007, 204:1757-1764.
14. Cros J., Cagnard N., Woollard K., Patey N., Zhang S.Y., Senechal B., Puel A., Biswas S.K., Moshous D., Picard C., et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 2010, 33:375-386.
15. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 2007, 8:1086-1094.
16. Edelson B.T., Kc W., Juang R., Kohyama M., Benoit L.A., Klekotka P.A., Moon C., Albring J.C., Ise W., Michael D.G., et al. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 2010, 207:823-836.
17. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
18. Grimm M.C., Pullman W.E., Bennett G.M., Sullivan P.J., Pavli P., Doe W.F. Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J. Gastroenterol. Hepatol. 1995, 10:387-395.
19. Hadis U., Wahl B., Schulz O., Hardtke-Wolenski M., Schippers A., Wagner N., Müller W., Sparwasser T., Förster R., Pabst O. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 2011, 34:237-246.
20. Irizarry R.A., Hobbs B., Collin F., Beazer-Barclay Y.D., Antonellis K.J., Scherf U., Speed T.P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003, 4:249-264.
21. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., Wei D., Goldfarb K.C., Santee C.A., Lynch S.V., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
22. Jaensson E., Uronen-Hansson H., Pabst O., Eksteen B., Tian J., Coombes J.L., Berg P.L., Davidsson T., Powrie F., Johansson-Lindbom B., Agace W.W. Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J. Exp. Med. 2008, 205:2139-2149.
23. Johansson-Lindbom B., Svensson M., Pabst O., Palmqvist C., Marquez G., Förster R., Agace W.W. Functional specialization of gut CD103+ dendritic cells in the regulation of tissue-selective T cell homing. J. Exp. Med. 2005, 202:1063-1073.
24. Jung S., Aliberti J., Graemmel P., Sunshine M.J., Kreutzberg G.W., Sher A., Littman D.R. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol. Cell. Biol. 2000, 20:4106-4114.
25. Jung S., Unutmaz D., Wong P., Sano G., De los Santos K., Sparwasser T., Wu S., Vuthoori S., Ko K., Zavala F., et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 2002, 17:211-220.
26. Kamada N., Hisamatsu T., Okamoto S., Chinen H., Kobayashi T., Sato T., Sakuraba A., Kitazume M.T., Sugita A., Koganei K., et al. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis. J. Clin. Invest. 2008, 118:2269-2280.
27. Kassiotis G., Kollias G. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 2001, 193:427-434.
28. Kobayashi K.S., Chamaillard M., Ogura Y., Henegariu O., Inohara N., Nuñez G., Flavell R.A. Nod2-dependent regulation of innate and adaptive immunity in the intestinal tract. Science 2005, 307:731-734.
29. Lin M.L., Zhan Y., Proietto A.I., Prato S., Wu L., Heath W.R., Villadangos J.A., Lew A.M. Selective suicide of cross-presenting CD8+ dendritic cells by cytochrome c injection shows functional heterogeneity within this subset. Proc. Natl. Acad. Sci. USA 2008, 105:3029-3034.
30. Liu K., Victora G.D., Schwickert T.A., Guermonprez P., Meredith M.M., Yao K., Chu F.F., Randolph G.J., Rudensky A.Y., Nussenzweig M. In vivo analysis of dendritic cell development and homeostasis. Science 2009, 324:392-397.
31. Meredith M.M., Liu K., Darrasse-Jeze G., Kamphorst A.O., Schreiber H.A., Guermonprez P., Idoyaga J., Cheong C., Yao K.H., Niec R.E., Nussenzweig M.C. Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J. Exp. Med. 2012, 209:1153-1165.
32. Mukhopadhyay S., Plüddemann A., Gordon S. Macrophage pattern recognition receptors in immunity, homeostasis and self tolerance. Adv. Exp. Med. Biol. 2009, 653:1-14.
33. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., Vyas J.M., Boes M., Ploegh H.L., Fox J.G., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005, 307:254-258.
34. Okayasu I., Hatakeyama S., Yamada M., Ohkusa T., Inagaki Y., Nakaya R. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990, 98:694-702.
35. Palframan R.T., Jung S., Cheng G., Weninger W., Luo Y., Dorf M., Littman D.R., Rollins B.J., Zweerink H., Rot A., von Andrian U.H. Inflammatory chemokine transport and presentation in HEV: a remote control mechanism for monocyte recruitment to lymph nodes in inflamed tissues. J. Exp. Med. 2001, 194:1361-1373.
36. Peterson D.A., McNulty N.P., Guruge J.L., Gordon J.I. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007, 2:328-339.
37. Platt A.M., Bain C.C., Bordon Y., Sester D.P., Mowat A.M. An independent subset of TLR expressing CCR2-dependent macrophages promotes colonic inflammation. J. Immunol. 2010, 184:6843-6854.
38. Powrie F., Leach M.W., Mauze S., Caddle L.B., Coffman R.L. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 1993, 5:1461-1471.
39. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
40. Rescigno M., Urbano M., Valzasina B., Francolini M., Rotta G., Bonasio R., Granucci F., Kraehenbuhl J.P., Ricciardi-Castagnoli P. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2001, 2:361-367.
41. Rivollier A., He J., Kole A., Valatas V., Kelsall B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 2012, 209:139-155.
42. Satpathy A.T., Kc W., Albring J.C., Edelson B.T., Kretzer N.M., Bhattacharya D., Murphy T.L., Murphy K.M. Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J. Exp. Med. 2012, 209:1135-1152.
43. Saunders D., Lucas K., Ismaili J., Wu L., Maraskovsky E., Dunn A., Shortman K. Dendritic cell development in culture from thymic precursor cells in the absence of granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1996, 184:2185-2196.
44. Schenk M., Bouchon A., Seibold F., Mueller C. TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J. Clin. Invest. 2007, 117:3097-3106.
45. Schulz O., Jaensson E., Persson E.K., Liu X., Worbs T., Agace W.W., Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 2009, 206:3101-3114.
46. Schulz C., Gomez Perdiguero E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., Prinz M., Wu B., Jacobsen S.E., Pollard J.W., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 2012, 336:86-90.
47. Serbina N.V., Pamer E.G. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 2006, 7:311-317.
48. Serbina N.V., Salazar-Mather T.P., Biron C.A., Kuziel W.A., Pamer E.G. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 2003, 19:59-70.
49. Shechter R., London A., Varol C., Raposo C., Cusimano M., Yovel G., Rolls A., Mack M., Pluchino S., Martino G., et al. Infiltrating blood-derived macrophages are vital cells playing an anti-inflammatory role in recovery from spinal cord injury in mice. PLoS Med. 2009, 6:e1000113.
50. Siddiqui K.R., Laffont S., Powrie F. E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated colitis. Immunity 2010, 32:557-567.
51. Smythies L.E., Sellers M., Clements R.H., Mosteller-Barnum M., Meng G., Benjamin W.H., Orenstein J.M., Smith P.D. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 2005, 115:66-75.
52. Swirski F.K., Nahrendorf M., Etzrodt M., Wildgruber M., Cortez-Retamozo V., Panizzi P., Figueiredo J.L., Kohler R.H., Chudnovskiy A., Waterman P., et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009, 325:612-616.
53. Travassos L.H., Girardin S.E., Philpott D.J., Blanot D., Nahori M.A., Werts C., Boneca I.G. Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 2004, 5:1000-1006.
54. Varol C., Landsman L., Fogg D.K., Greenshtein L., Gildor B., Margalit R., Kalchenko V., Geissmann F., Jung S. Monocytes give rise to mucosal, but not splenic, conventional dendritic cells. J. Exp. Med. 2007, 204:171-180.
55. Varol C., Vallon-Eberhard A., Elinav E., Aychek T., Shapira Y., Luche H., Fehling H.J., Hardt W.D., Shakhar G., Jung S. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009, 31:502-512.
56. Varol C., Zigmond E., Jung S. Securing the immune tightrope: mononuclear phagocytes in the intestinal lamina propria. Nat. Rev. Immunol. 2010, 10:415-426.
57. Waddell A., Ahrens R., Steinbrecher K., Donovan B., Rothenberg M.E., Munitz A., Hogan S.P. Colonic eosinophilic inflammation in experimental colitis is mediated by Ly6C(high) CCR2(+) inflammatory monocyte/macrophage-derived CCL11. J. Immunol. 2011, 186:5993-6003.
58. Weber B., Saurer L., Schenk M., Dickgreber N., Mueller C. CX3CR1 defines functionally distinct intestinal mononuclear phagocyte subsets which maintain their respective functions during homeostatic and inflammatory conditions. Eur. J. Immunol. 2011, 41:773-779.
59. Zigmond E., Halpern Z., Elinav E., Brazowski E., Jung S., Varol C. Utilization of murine colonoscopy for orthotopic implantation of colorectal cancer. PLoS ONE 2011, 6:e28858.